Distinct Brain Areas involved in Anger versus Punishment during Social Interactions

Abstract

Although anger and aggression can have wide-ranging consequences for social interactions, there is sparse knowledge as to which brain activations underlie the feelings of anger and the regulation of related punishment behaviors. To address these issues, we studied brain activity while participants played an economic interaction paradigm called Inequality Game (IG). The current study confirms that the IG elicits anger through the competitive behavior of an unfair (versus fair) other and promotes punishment behavior. Critically, when participants see the face of the unfair other, self-reported anger is parametrically related to activations in temporal areas and amygdala - regions typically associated with mentalizing and emotion processing, respectively. During anger provocation, activations in the dorsolateral prefrontal cortex, an area important for regulating emotions, predicted the inhibition of later punishment behavior. When participants subsequently engaged in behavioral decisions for the unfair versus fair other, increased activations were observed in regions involved in behavioral adjustment and social cognition, comprising posterior cingulate cortex, temporal cortex, and precuneus. These data point to a distinction of brain activations related to angry feelings and the control of subsequent behavioral choices. Furthermore, they show a contribution of prefrontal control mechanisms during anger provocation to the inhibition of later punishment.

Figure 1

Study design. (a) The three phases of the Inequality Game (given in successive scanning runs). (b) Depiction of event frames of a single trial in the high power phase with their respective duration. Each time the participant is paired with one of the two other players, a screen is displayed that reads “Selection of participants”. Then, participants see a photograph of the other (fair or unfair) that is accompanied with the information that this player controls the columns in the high power phase (and the lines in the low power phase). This is followed by the display of the payoff matrix determining the distribution of gains for the two current players (“New Trial”), the decision screen for the person in high power (“Decision Lines”), the display of this decision (“Result Lines”), a display indicating that the other person is deciding (“Decision Columns”), and lastly the display of the other’s decision which serves at the final outcome display (“Final Result”). In the current example, the player with high power (here: Nicolas, in green) begins by selecting a line in the matrix, which is followed by the choice of the low power player (here: Jean, in blue) who selects a column. The intersection of their choice determines the final gain allocated to each player (here a competitive distribution is depicted in which Nicolas earns 8 CHF and Jean earns 1 CHF). Then, the player with high power can select one of four feedback messages for the other player.

Figure 2

Effects of anger provocation in the low power phase on self-reported emotions and behavior. (a) Self-reported feelings in response to the fair other’s cooperative choice and the unfair other’s competitive choice in the low power phase. Bars depict means and + /−1 standard error. Asterisks refer to follow-up comparisons with **P < 0.01; ***P < 0.001. (b) Participants’ economic behavior towards the fair and unfair other in the high power phase at baseline and the high power phase following provocation. Bars depict means and + /−1 standard error. Asterisks show the results of follow-up pairwise comparisons with **P < 0.01.

Figure 3

(a) Activations in right amygdala when seeing the unfair other’s face during the low power phase with provocation are parametrically modulated by self-reported feelings of anger. (b) Activations in bilateral dorsolateral prefrontal cortex (DLPFC) when seeing the face of the unfair other during the low power phase predicted the inhibition of punishment behavior during the subsequent high power phase. R, right.

Figure 4

Activations in superior temporal gyrus, dorsolateral prefrontal cortex, posterior cingulate cortex and precuneus when participants make relevant economic choices for the unfair other as opposed to the fair other in the high power phase after provocation minus the high power phase at baseline (for details, see Supplementary Table 10). Numbers indicate MNI coordinates of the shown slices.